Diet of Rhinolophus Hipposideros During Breeding Season in the South-Western Italian Alps
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Vespertilio 18: 29–39, 2016 ISSN 1213-6123 Diet of Rhinolophus hipposideros during breeding season in the south-western Italian Alps Stefania Bono & Roberto Toffoli CHIROSPHERA Associazione per lo studio e la tutela dei Chirotteri e l’ambiente, Via Tetti Barbiere 11, 10026, Santena TO, Italy; [email protected] Abstract. We studied the diet of the lesser horseshoe bat Rhinolophus hipposideros at seven breeding colonies in the south-western Italian Alps: three colonies in the province of Cuneo (Piedmont), and four in the province of Imperia (Ligury). The analysis was based on 210 bat droppings, which were collected during two field campaigns that took place in the period between June and August 2008 and 2009, respectively. We identified members of the following groups of arthropods: Acarina, Lepidoptera, Diptera, Hymenoptera, Neuroptera, Coleoptera, Hemiptera and Chilopoda. According to the calculated frequency, occurrence and volume percentages, the most important prey items are Lepidoptera and Diptera. These two taxa seem to dominate the diet of Rhinolophus hipposideros all across Europe. To cover its food requirements, it seems that Rhinolophus hipposideros needs areas with mature forest vegetation, especially near waterways or wetlands, and the presence of pastures for hunting during the reproductive period. Rhinolophus hipposideros, diet, prey, food habits, Italian Alps Introduction The study of the diet of chiropterans based on the observation of tracks in droppings is conside- red a reliable method both from the qualitative and quantitative point of view (Kunz & Whitaker 1983). Despite uncertainties, this analysis provides information on the frequency of occurrence of individual prey items and an estimation of the mean volume of each prey item in the whole sample (Whitaker et al. 2009). However, it is important to mention the difficulties that this method of work involves, especially in the determination of the remains due to a high degree of digestion and mastication. For this reason, determination of the fragments of arthropods has mainly been made at the level of order, while the family can be identified only in few cases. Nonetheless, guano analysis provides a fair picture of the variety of types of prey consumed by insectivorous species (Kunz & Whitaker 1983, Dickman & Huang 1988, McAney et al. 1991, Roué 1999). The aim of this contribution is to increase the knowledge on the diet of Rhinolophus hipposi- deros (Borkhausen, 1797) in the breeding season in the south-western Alps; as such information is entirely missing. The existing studies on the diet of Rhinolophus hipposideros have been carried out in European areas with a climate and vegetation typical for the temperate region and Mediterranean mountains: western Ireland (McAney & Fairley 1989), France (Lorraine) (Artois et al.1990), Switzerland (Godat et al. 1991, Beck 1995), Belgium and Luxembourg (Motte 1998), Britain (Leishman 1983, Williams et al. 2011), and Portugal (Lino et al. 2014). No data have been gathered on the diet of Rhinolophus hipposideros in the southern Alps. The research conducted in western Ireland showed that the diet of Rhinolophus hipposideros consists primarily of insects belonging to nematoceran Diptera (McAney & Fairley 1989). In 29 western Ireland, 23 families of insects belonging to seven different orders were identified: Le- pidoptera, Neuroptera, Trichoptera, Hymenoptera, Coleoptera, Diptera, Hemiptera and Araneae. In general, there are nine orders of arthropods known to be a part of the diet of Rhinolophus hipposideros: Psocoptera, Hemiptera, Neuroptera, Coleoptera, Diptera, Lepidoptera, Trichoptera, Hymenoptera, and Araneae (Poulton 1929, Leishman 1983, McAney & Fairley 1989, Hollyfield 1993, Beck et al. 1989, Beck 1995, Artois et al. 1990, Godat et al. 1991, Williams et al. 2011, Motte 1998, Lino et al. 2014). In this study we analyzed the diet of a population of Rhinolophus hipposideros in the south- -western Italian Alps between Ligury and Piedmont. Specifically, we aimed to characterize the diet of Rhinolophus hipposideros in this region and compare the diet between the two areas. Material and Methods Seven mono-specific breeding colonies of Rhinolophus hipposideros were studied. Three (Demonte, Valdieri and Bag- nasco) were located in the province of Cuneo (Piedmont) and four (Badalucco, Molini di Triora, Triora and Baiardo) in the province of Imperia (Ligury) in the north-west of Italy (Fig. 1). The studied colonies consist of a minimum of 9 to a maximum of 56 females (Table 1). The Piedmont colonies are located at the bottom of a wide valley of the Po basin, characterized by large forested areas alternating with grasslands, pastures and riparian habitats. In the Ligurian landscape there are narrow furrows, which are mainly characterized by extensive forest areas (Table 2). For each site, 30 dropping samples (i.e. 210 total) were collected during two field campaigns directly under the bat roost sites in the period between June and August 2008 and 2009, respectively. The guano was stored in plastic containers kept open for 24 hours to allow the Fig. 1. The area under study and the Rhinolophus hipposideros colonies studied. Obr. 1. Studované území a studované kolonie vrápence malého (Rhinolophus hipposideros). 30 Table 1. List of the studied breeding colonies of Rhinolophus hipposideros and the number of the adult females observed Tab. 1. Soupis studovaných mateřských kolonií vrápence malého (Rhinolophus hipposideros) a počet pozo- rovaných dospělých samic region locality province altitude number ♀♀ region lokalita provincie nadmořská výška počet ♀♀ [m a. s. l. / m n. m.] Piedmont Demonte Cuneo 849 35 Piedmont Valdieri Cuneo 758 9 Piedmont Bagnasco Cuneo 847 13 Ligury Badalucco Imperia 295 56 Ligury Molini di Triora Imperia 440 37 Ligury Triora Imperia 750 18 Ligury Baiardo Imperia 690 35 desiccation of the material and avoid the formation of mould. About 24 hours before the observation under the microscope, the excrements were put into Eppendorf tubes (2 ml) filled with 70% alcohol (Whitaker et al. 2009). All fecal pellets were soaked in glycerol in order to be softened, crushed with tweezers and placed under the stereomi- croscope for the determination of the fragments of arthropods. For identification, the fragments were separated from the rest, cleaned in water, and eventually placed once more in Eppendorf tubes filled with 70% alcohol. The determination of the fragments was carried out based on the studies by Beck (1995) and Shiel et al. (1997) and specimens preserved in entomological collections (MCCI – Museo Civico di Storia Naturale di Carmagnola; MRSN – Museo Regionale di Scienza Naturali di Torino). When the determination was questionable, the term “cfr.” (namely “compare”) was applied. The results were expressed as in Vaughan (1997): volume percentages: the percentage estimate of volume of the remains of each taxon in each sample of guano (total=100%). In the present study, the estimation of the volume was not based on an appreciation in classes of 5%, but on the number of fragments belonging to different members of the taxon found in the excrement occurrence percentage: the percentage of fecal pellets examined containing each prey taxon (total>100%); frequency percentage: the number of taxon occurrences (i.e. the number of pellets which contained it), divided by the total number of occurrences, multiplied by 100 (total=100%). The differences between the results were analyzed using the chi-square distribution (χ2) and multivariate analysis (ANOVA) after transformation of the percentages of arcsin volumes as shown by Whittaker et al. (2009). The diversity of the diet of each colony was estimated using the Shannon-Weaver index of diversity (Krebs 1999). The Mann-Whitney U-test (Z) was performed to calculate the difference between the values of diversity obtained in various localities, and Table 2. Percentage of habitats present in a radius of 5 km from the colony roosts and distance to rivers; AA = % agricultural areas, WSA = % wooded and seminaturals areas, UA = % urban areas, DR = distance to rivers in meters (APAT 2005) Tab. 2. Procentuální zastoupení jednotlivých biotopů v kruhu o poloměru 5 km kolem úkrytu kolonie a vzdálenost úkrytu od řeky; AA = % zemědělské plochy, WSA = % lesní a polopřirozené plochy, UA = % osídlené plochy, DR = vzdálenost k řece v metrech (APAT 2005) region locality / lokalita AA WSA UA DR Ligury Molini di Triora 4.1 95.9 293 Triora 1.8 98.2 198 Baiardo 16.8 82.9 0.13 321 Badalucco 8.5 91.5 470 Piedmont Bagnasco 15.3 83.6 1.13 259 Valdieri 13.8 82.9 3.30 478 Demonte 19.6 79.7 0.76 808 31 Table 3. Occurrence, percentage occurrence, percentage frequency and volume percentage for each taxon in the Rhinolophus hipposideros diet recorded in Piedmont and Ligury Tab. 3. Výskyt (počet kusů trusu s výskytem taxonu), procentuální výskyt, procentuální četnost a procentuální objem každého taxonu zjištěného v potravě vrápence malého (Rhinolophus hipposideros ) zjištěné v Piemontu a Ligurii taxon region occurrence % occurrence % frequency % volume výskyt % výskytu % četnosti % objemu Acarina Piedmont 10 11.11 3.7 0.9 Ligury 4 3.3 1.3 0.4 Lepidoptera Piedmont 86 95.7 31.4 35.9 Ligury 116 96.7 38.2 52.7 Diptera Piedmont 87 96.7 31.8 45.2 Ligury 95 79.2 31.3 30.6 Hymenoptera Piedmont 34 37.8 12.4 7.1 Ligury 31 25.8 10.2 5.7 Neuroptera Piedmont 33 36.7 12.0 7.2 Ligury 31 25.8 10.2 5.8 Coleoptera Piedmont 15 16.7 5.5 2.7 Ligury 15 12.5 4.9 3.4 Heteroptera Piedmont 9 10.0 3.3 0.9 Ligury 11 9.2 3.6 1.3 Chilopoda Piedmont 0 0.0 0.0 0.0 Ligury 1 0.8 0.3 0.0 to measure the difference between the number of taxa in Piedmont and Ligury. Finally, the correlation was carried out using the Spearman’s rank correlation (Rs) between the volume percentage of main prey identified compared to some environmental variables present in a 5 km radius from the colonies (Table 2), considering this as a maximum distance of movements between roosts and hunting areas (Bontadina et al.